Gut Microbial Diversity and Ecological Specialization in Four Sympatric Lemur Species Under Lean Conditions

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2021-12-01

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Abstract

The gut microbiome is gaining recognition for its role in primate nutrition, but we stand to benefit from microbiome comparisons across diverse hosts and environmental conditions. We compared gut microbiome structure in four lemur species from four phylogenetic lineages, including 9 individual mouse lemurs (Microcebus danfossi), 6 brown lemurs (Eulemur fulvus), 20 sifakas (Propithecus coquereli), and a single sportive lemur (Lepilemur grewcockorum). In northwestern Madagascar, these species are sympatric, but use different feeding strategies to cope with environmental challenges, including relying on tree gums and insects (mouse lemurs), and some vs. significant leaf matter (brown lemurs vs. sifakas and sportive lemurs). From one fecal sample collected per lemur in the dry season in the Anjajavy Forest, we determined gut microbiome diversity, variability, and membership via 16S rRNA sequencing. The lemurs harbored strongly species-specific gut microbiomes. Brown lemurs showed more diverse and generalized consortia; mouse lemurs, sifakas, and the sportive lemur had less diverse consortia with more distinct memberships. Consistent with their fallback foods, mouse lemur microbiomes included taxa putatively associated with gum and insect digestion, whereas those of sifakas and the sportive lemur showed stronger and distinct signatures of leaf fiber and secondary compound metabolism. These results point to feeding strategy, intertwined with host phylogeny, as a driver of gut microbiome composition, but highlight real-time dietary specificity as a contributing driver of microbiome diversity. While illuminating how gut microbiomes facilitate host nutrition on challenging foods, these results help explain how ecologically diverse primates living in sympatry may differentially cope with seasonal or stochastic lean times.

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10.1007/s10764-021-00257-9

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Greene, LK, E Rambeloson, HA Rasoanaivo, ED Foss, AD Yoder, CM Drea and MB Blanco (2021). Gut Microbial Diversity and Ecological Specialization in Four Sympatric Lemur Species Under Lean Conditions. International Journal of Primatology, 42(6). pp. 961–979. 10.1007/s10764-021-00257-9 Retrieved from https://hdl.handle.net/10161/28429.

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Scholars@Duke

Greene

Lydia Greene

Dir, Acad Engagement for Acad Discipline

I am currently the Director of Academic Engagement for the Natural & Quantitative Sciences in Duke's Academic Advising Center, where I serve as a specialized advisor for our STEM undergraduates. I am also Adjunct Faculty in the Department of Biology, where I teach, mentor, and research. 

My research is on the ecology of lemurs in Madagascar, with a central focus on mechanisms of local adaptation in sifakas and biogeography of mouse and dwarf lemurs. Prior to my current position, I was a postdoctoral associate at the Duke Lemur Center and graduate student in Duke's Ecology Program. My dissertation research was on the role of the gut microbiome in facilitating folivory as an ecological strategy in lemurs.

Yoder

Anne Daphne Yoder

Braxton Craven Distinguished Professor of Evolutionary Biology

My work integrates field inventory activities with molecular phylogenetic techniques and geospatial analysis to investigate Madagascar, an area of the world that is biologically complex, poorly understood, and urgently threatened. Madagascar has been designated as one of the most critical geographic priorities for conservation action, retaining less than 10% of the natural habitats that existed before human colonization. It is critical that information be obtained as quickly as possible to document the biota that occurs in the remaining and highly threatened forested areas of western Madagascar, to gain an understanding of the evolutionary processes and associated distributional patterns that have shaped this diversity, and to use this information to help set conservation priorities. Phylogenetic and biogeographic analysis of Malagasy vertebrates, each with unique life-history and dispersal characteristics, are conducted to identify areas of high endemism potentially associated with underlying geological features, and also to test for the role that geographic features have played in generating patterns of vertebrate diversity and distribution. My lab also has a significant focus on capacity-building through the education and training of both American and Malagasy students. Research opportunities for American graduate students are enhanced by the formation of Malagasy/American partnerships.

Drea

Christine M. Drea

Professor in the Department of Evolutionary Anthropology

I have two broad research interests, sexual differentiation and social behavior, both focused on hyenas and primates. I am particularly interested in unusual species in which the females display a suite of masculinized characteristics, including male- like or exaggerated external genitalia and social dominance.
The study of naturally occurring hormones in such unique mammals can reveal general processes of hormonal activity, expressed in genital morphology, reproductive development, and social behavior. Taking a combined laboratory and field approach allows me to relate captive data to various facets of the animals' natural habitat, thereby enhancing the ecological validity of assay procedures and enriching interpretation in an evolutionary framework. The goal of comparative studies of hyenas and lemurs is to help elucidate the mechanisms of mammalian sexual differentiation.

My research program in social behavior focuses on social learning and group cohesion. Using naturalistic tasks that I present to captive animals in socially relevant contexts, I can investigate how social interaction modulates behavior, problem- solving, and cognitive performance. By studying and comparing models of carnivore and primate foraging, I can better understand how group-living animals modify their actions to meet environmental demands. A primary interest is determining whether similar factors, related to having a complex social organization, influence learning and performance across taxonomic groups. I am also interested in how animals learn rules of social conduct and maintain social cohesion, as evidenced by their patterns of behavioral developmental, the intricate balance between aggression and play, the expression of scent marking, and the social facilitation or inhibition of behavior.

Marina Blanco

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